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Coral reefs are biodiversity hotspots, places of high endemicity and provide essential services to billions of people globally. With increasing threats to these reefs worldwide, there is a need to implement faster, more efficient ways to monitor spatial and temporal patterns of biodiversity. Environmental DNA (eDNA) metabarcoding offers a promising tool to address this issue, as it has revolutionized our ability to monitor biodiversity from complex environmental samples such as seawater. However, the capacity for eDNA to resolve fine scale shifts in community composition across habitats in seascapes is yet to be fully explored. Here, we applied eDNA metabarcoding using the rRNA 18S Universal eukaryote assay to explore differences in community profiles between samples collected from the lagoon and reef slope habitats across more than 170 km of the Ningaloo Coast World Heritage Area in Western Australia. We recovered 2061 amplicon sequence variants that comprised of 401 taxa spanning 14 different metazoan phyla such as cnidarians, poriferans, molluscs, algae, worms, and echinoderms. Our results revealed strong clustering of samples by habitat type across the length of the reef. Community dissimilarity (beta diversity) between samples collected from the reef slope and lagoon habitats was high and was driven largely by a strong rate of spatial turnover, indicating a distinct set of taxa representing each reef zone community. We also detected a strong pattern of isolation by distance within our slope samples, suggesting that communities are spatially stratified across the length of the reef. Despite high connectivity due to regular flushing of the lagoon environment, our results demonstrate that metabarcoding of seawater eDNA from different habitats can resolve fine scale community structure. By generating multi-trophic biodiversity data, our study also provided baseline data for Ningaloo from which future changes can be assessed.

The need for efficient and more accurate ways of monitoring threatened ecosystems is becoming increasingly urgent as climate change intensifies. Coral reefs are an example of an ecosystem in crisis, with widespread declines in coral cover and diversity documented over recent decades. Novel molecular approaches such as biomonitoring using environmental DNA (eDNA) from seawater samples show great potential to complement future coral reef monitoring programs, especially when used in combination with conventional methods. However, eDNA metabarcoding studies often rely on public databases (e.g., GenBank) for assigning taxonomy, which generally limits the number of sequences that can be taxonomically identified. The extent to which building reference tissue sequences improves taxonomic resolution has yet to be fully examined. Here, we combined traditional coral reef monitoring data with eDNA assessments derived from seawater collected at the highly diverse Rowley Shoals in Western Australia. Using two ITS2 assays developed to target basal metazoan DNA and a reference database spiked with 70 local coral specimens, we identified 37 genera and 40 species from 56 1 L seawater samples. We identified considerable overlap of taxa with visual survey data and showed that assignment of amplicon sequence variants was significantly improved when “spiking” the taxonomic classifier with curated sequences of locally collected species. Our findings showcase the potential of eDNA metabarcoding for monitoring the biodiversity of reef corals and highlight the importance of custom reference sequence databases for improving taxonomic resolution in metabarcoding studies.

At the Rowley Shoals in Western Australia, the prominent reef flat becomes exposed on low tide and the stagnant water in the shallow atoll lagoons heats up, creating a natural laboratory for characterizing the mechanisms of coral resilience to climate change. To explore these mechanisms in the reef coral Acropora tenuis , we collected samples from lagoon and reef slope habitats and combined whole-genome sequencing, ITS2 metabarcoding, experimental heat stress, and transcriptomics. Despite high gene flow across the atoll, we identified clear shifts in allele frequencies between habitats at relatively small linked genomic islands. Common garden heat stress assays showed corals from the lagoon to be more resistant to bleaching, and RNA sequencing revealed marked differences in baseline levels of gene expression between habitats. Our results provide new insight into the complex mechanisms of coral resilience to climate change and highlight the potential for spatially varying selection across complex coral reef seascapes to drive pronounced ecological divergence in climate-related traits.

Understanding the mechanisms driving phenotypic variation in traits facing intensified selection from climate change is a crucial step in developing effective conservation and restoration initiatives. This is particularly true for reef-building corals, which are among the most vulnerable to climate change and are in dramatic decline globally. At the Rowley Shoals in Western Australia, the prominent reef flat becomes exposed on low tide and the stagnant water in the shallow atoll lagoons heats up, creating a natural laboratory for characterising the mechanisms that control phenotypic responses to different environments. We combined whole genome re-sequencing, common garden heat stress experiments, transcriptome-wide gene expression analyses, and symbiont metabarcoding to explore the mechanisms that facilitate survival in contrasting habitat conditions. Our data show that, despite high gene flow between habitats, spatially varying selection drives subtle shifts in allele frequencies at hundreds of loci. These changes were concentrated into several islands of divergence spanning hundreds of SNPs that showed strong linkage disequilibrium and were associated with a coordinated increase in minor allele frequencies in corals taken from the lagoon habitat, where the range of environmental conditions is greatest. Common garden heat stress assays showed individuals from the lagoon exhibited higher bleaching resistance than colonies from the reef slope, and RNAseq identified pronounced physiological differences between the corals from the two habitats, primarily associated with molecular pathways including cell signalling, ion transport and metabolism. Despite the pronounced physioloigical and environmental differences between habitats, metabarcoding of theSymbiodiniaceaeITS2 region revealed all colonies to be associated exclusively with the genusCladocopium, with no detectable differences between habitats. This study contributes to the growing number of studies documenting the complex mechanisms that facilitate coral survival in extreme environments, and showcases the utility of combining multiple sequencing techniques to unravel complex climate-related traits.

Naturally heat-resistant coral populations hold significant potential for facilitating coral reef survival under rapid climate change. However, it remains poorly understood whether they can acclimatize to ocean warming when superimposed on their already thermally-extreme habitats. Furthermore, it is unknown whether they can maintain their heat tolerance upon larval dispersal or translocation to cooler reefs. We test this in a long-term mesocosm experiment using stress-resistant corals from thermally-extreme reefs in NW Australia. We show that these corals have a remarkable ability to maintain their heat tolerance and health despite acclimation to 3–6 °C cooler, more stable temperatures over 9 months. However, they are unable to increase their bleaching thresholds after 6-months acclimation to + 1 °C warming. This apparent rigidity in the thermal thresholds of even stress-resistant corals highlights the increasing vulnerability of corals to ocean warming, but provides a rationale for human-assisted migration to restore cooler, degraded reefs with corals from thermally-extreme reefs., Coral populations from thermally extreme conditions may help restore reefs degraded by bleaching. Here, the authors show that these corals can maintain their heat tolerance despite acclimation to colder temperatures but have a limited capacity to acclimatize to ocean warming.